Genotype-by-Environment Effects of Cis-Variations in the Atgl Promoter Mediate the Divergent Pattern of Phenotypic Plasticity for Temperature Adaptation in Two Congeneric Oyster Species

Abstract

Phenotypic plasticity plays an essential role in adaptive evolution. However, the molecular mechanisms of how genotype-by-environment interaction (G × E) effects shape phenotypic plasticity in marine organisms remain poorly understood. The crucial temperature-responsive trait triacylglycerol (TAG) content and its major gene adipose triglyceride lipase (Atgl) expression have divergent plastic patterns in two congeneric oyster species (Crassostrea gigas and Crassostrea angulata) to adapt to relative-cold/northern and relative-warm/southern habitats, respectively. In this study, eight putative loci were identified in the Atgl promoter region (cis-variations) between wild C. gigas and C. angulata that exhibited differential environmental responsiveness (G × E). The G and G × E effects of each locus were further dissected by measuring the Atgl gene expression of different genotypes in response to temperature changes at the cellular and organismal levels. Two transcription factors, non-environmentally responsive non-POU domain-containing octamer-binding protein (Nono) and environmentally responsive heterogeneous nuclear ribonucleoprotein K (Hnrnpk), were screened for binding to g.-1804 (G locus) and g.-1919 (G + G × E locus), respectively. The specificity of Nono binding to the C. angulata allele mediated the G effects of g.-1804, and the lower environmental sensitivity of Hnrnpk in C. angulata mediated the G × E effects of g.-1919, jointly regulating the trade-offs between higher constitutive and lower plastic expression of Atgl gene expression in C. angulata. This study served as an experimental case to reveal how the genetic variations with G and (or) G × E effects propagate into the divergent pattern of plasticity in environmental adaptive traits, which provides new insights into predicting the adaptability of marine organisms to future climate changes.